Convergent molecular evolution of phosphoenolpyruvate carboxylase gene family in C4 and crassulacean acid metabolism plants

Phosphoenolpyruvate carboxylase (PEPC), as the key enzyme in initial carbon fixation of C4and crassulacean acid mechanism (CAM) pathways, was thought to undergo convergent adaptive changes resulting in the convergent evolution of C4 and CAM photosynthesis in vascular plants. However, the integral ev...

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Main Authors: Jiang-Ping Shu, Yue-Hong Yan, Rui-Jiang Wang
Format: Article
Language:English
Published: PeerJ Inc. 2022-01-01
Series:PeerJ
Subjects:
Online Access:https://peerj.com/articles/12828.pdf
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author Jiang-Ping Shu
Yue-Hong Yan
Rui-Jiang Wang
author_facet Jiang-Ping Shu
Yue-Hong Yan
Rui-Jiang Wang
author_sort Jiang-Ping Shu
collection DOAJ
description Phosphoenolpyruvate carboxylase (PEPC), as the key enzyme in initial carbon fixation of C4and crassulacean acid mechanism (CAM) pathways, was thought to undergo convergent adaptive changes resulting in the convergent evolution of C4 and CAM photosynthesis in vascular plants. However, the integral evolutionary history and convergence of PEPC in plants remain poorly understood. In the present study, we identified the members of PEPC gene family across green plants with seventeen genomic datasets, found ten conserved motifs and modeled three-dimensional protein structures of 90 plant-type PEPC genes. After reconstructing PEPC gene family tree and reconciled with species tree, we found PEPC genes underwent 71 gene duplication events and 16 gene loss events, which might result from whole-genome duplication events in plants. Based on the phylogenetic tree of the PEPC gene family, we detected four convergent evolution sites of PEPC in C4 species but none in CAM species. The PEPC gene family was ubiquitous and highly conservative in green plants. After originating from gene duplication of ancestral C3-PEPC, C4-PEPC isoforms underwent convergent molecular substitution that might facilitate the convergent evolution of C4 photosynthesis in Angiosperms. However, there was no evidence for convergent molecular evolution of PEPC genes between CAM plants. Our findings help to understand the origin and convergent evolution of C4 and CAM plants and shed light on the adaptation of plants in dry, hot environments.
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spelling doaj.art-ee8da107681745e6ad340f7bfcdf61f82023-12-02T21:50:22ZengPeerJ Inc.PeerJ2167-83592022-01-0110e1282810.7717/peerj.12828Convergent molecular evolution of phosphoenolpyruvate carboxylase gene family in C4 and crassulacean acid metabolism plantsJiang-Ping Shu0Yue-Hong Yan1Rui-Jiang Wang2Key laboratory of Plant Resources Conservation and Sustainable Utilization, South China Botanical Garden, Chinese Academy of Sciences, Guangzhou, ChinaKey Laboratory of National Forestry and Grassland Administration for Orchid Conservation and Utilization, The National Orchid Conservation Centre of China and The Orchid Conservation and Research Centre of Shenzhen, Shenzhen, ChinaKey laboratory of Plant Resources Conservation and Sustainable Utilization, South China Botanical Garden, Chinese Academy of Sciences, Guangzhou, ChinaPhosphoenolpyruvate carboxylase (PEPC), as the key enzyme in initial carbon fixation of C4and crassulacean acid mechanism (CAM) pathways, was thought to undergo convergent adaptive changes resulting in the convergent evolution of C4 and CAM photosynthesis in vascular plants. However, the integral evolutionary history and convergence of PEPC in plants remain poorly understood. In the present study, we identified the members of PEPC gene family across green plants with seventeen genomic datasets, found ten conserved motifs and modeled three-dimensional protein structures of 90 plant-type PEPC genes. After reconstructing PEPC gene family tree and reconciled with species tree, we found PEPC genes underwent 71 gene duplication events and 16 gene loss events, which might result from whole-genome duplication events in plants. Based on the phylogenetic tree of the PEPC gene family, we detected four convergent evolution sites of PEPC in C4 species but none in CAM species. The PEPC gene family was ubiquitous and highly conservative in green plants. After originating from gene duplication of ancestral C3-PEPC, C4-PEPC isoforms underwent convergent molecular substitution that might facilitate the convergent evolution of C4 photosynthesis in Angiosperms. However, there was no evidence for convergent molecular evolution of PEPC genes between CAM plants. Our findings help to understand the origin and convergent evolution of C4 and CAM plants and shed light on the adaptation of plants in dry, hot environments.https://peerj.com/articles/12828.pdfPEPCConvergent evolutionCarbon-concentrating mechanismsPhotosynthetic convergencePhylogeny
spellingShingle Jiang-Ping Shu
Yue-Hong Yan
Rui-Jiang Wang
Convergent molecular evolution of phosphoenolpyruvate carboxylase gene family in C4 and crassulacean acid metabolism plants
PeerJ
PEPC
Convergent evolution
Carbon-concentrating mechanisms
Photosynthetic convergence
Phylogeny
title Convergent molecular evolution of phosphoenolpyruvate carboxylase gene family in C4 and crassulacean acid metabolism plants
title_full Convergent molecular evolution of phosphoenolpyruvate carboxylase gene family in C4 and crassulacean acid metabolism plants
title_fullStr Convergent molecular evolution of phosphoenolpyruvate carboxylase gene family in C4 and crassulacean acid metabolism plants
title_full_unstemmed Convergent molecular evolution of phosphoenolpyruvate carboxylase gene family in C4 and crassulacean acid metabolism plants
title_short Convergent molecular evolution of phosphoenolpyruvate carboxylase gene family in C4 and crassulacean acid metabolism plants
title_sort convergent molecular evolution of phosphoenolpyruvate carboxylase gene family in c4 and crassulacean acid metabolism plants
topic PEPC
Convergent evolution
Carbon-concentrating mechanisms
Photosynthetic convergence
Phylogeny
url https://peerj.com/articles/12828.pdf
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